Prevalence of Healthcare-Associated Infections in a Tertiary Hospital in Casablanca, Morocco, 2021

Background: During the COVID-19 pandemic, healthcare professionals experienced an increased workload, which may have affected infection prevention and control (IPC) programs and consequently healthcare-associated infection (HAI) rates. The objective of this study was to estimate the prevalence of HAI in Ibn Rochd University Hospital Center (IRUHC) and identify associated factors. Methods: A survey was conducted on November 30, 2021 at IRUHC, including all patients hospitalized for at least 48 hours. Data was collected using a questionnaire, and analyzed using SPSS IBM software version 16. The significance level was set at 0.05. Results: Among 887 patients, the prevalence of HAI was 9.7% (7.7%; 11.6%). The highest prevalence was observed in intensive care units (ICUs) (44.2%). Nosocomial pneumonia was the most common site (26.8%). The main isolated microorganisms were Acinetobacter baumannii (18.0%) and Escherichia coli (16.0%). All Acinetobacter baumannii isolated strains were imipenem-resistant. The presence of HAI was significantly associated with the presence of an invasive medical device (p<0.001), a higher physical status score of American Society of Anesthesiologists (ASA) (p<0.001), and a longer hospital stay (p<0.001). Conclusion : The emergence of imipenem-resistant Acinetobacter baumannii (IRAB) represents a serious therapeutic and epidemiological problem requiring the establishment of a system for monitoring the microbial environment and the application of strict hygiene measures.


Introduction
Healthcare-associated infections (HAIs) continue to burden healthcare systems with excess morbidity, mortality, and additional financial cost [1].According to World Health Organization (WHO), 7% of patients in acute-care hospitals in high-income countries and 15% in low-and middle-income countries will acquire at least one HAI during their hospital stay.On average,10% of affected patients will die from their HAI [2].
An HAI is an infection that is acquired by a patient during care delivery in a hospital or other healthcare facilities and was not present or incubating on admission [3].These infections are mostly caused by microorganisms resistant to one or more commonly-used antibiotics [3].They can be associated with devices used in medical procedures, such as catheters or ventilators.Common HAIs include central line-associated bloodstream infections (BSIs), catheter-associated urinary tract infections, ventilator-associated pneumonia, and surgical site infections (SSIs) [4].
Before the pandemic, HAI prevention and control interventions showed progress in reducing HAI rates and other adverse outcomes [5,6].
The COVID-19 pandemic has significantly affected healthcare systems globaly.Healthcare professionals experienced high levels of burnout during the pandemic due to increased workload [7,8].This may have affected infection prevention and control (IPC) programs and consequently HAI rates.Data from the USA National Healthcare Safety Network (NHSN) showed significantly higher incidence of different types of HAI in 2021 compared to 2019 [9].

Study design and setting
A cross-sectional point prevalence survey was conducted on November 30th,2021 in three institutions of IRUHC, Casablanca, Morocco.

Study population
The study included all patients who were hospitalized for at least 48 hours in one of the IRUHC departments and who were present on the day of the survey.
Newborns who were less than two days old, patients admitted for emergency observation, patients in day hospitals and patients in dental centers were excluded from the study.

Data collection procedure
Data was collected using a questionnaire by residents and nurses who had received a training before the survey day.Data was collected from medical records with the support of the attending physician and nurse.

Variables
The questionnaire presented two sections.The first section included patients general information (age, gender, length of stay, immunosuppression, American Society of Anesthesiologists (ASA) score, presence of invasive medical device, surgical procedure, etc.).The second section was intended only for patients who had an HAI (site of infection, isolated germs, etc.).
The criteria for defining a healthcare-associated infection were based on definitions proposed by the WHO [10].An HAI is defined as an infection acquired during a hospital stay and occurring more than 48 hours after admission.The diagnosis of respiratory infection was suggested in the presence of respiratory symptoms with at least two of the following signs appearing during hospitalization: cough, purulent sputum, new infiltration visible on chest X-ray and compatible with the diagnosis of infection.The diagnosis of SSI was suggested in the presence of any purulent discharge, surgical abscess or extensive cellulitis on the surgical site in the month following surgery.A positive urine culture (one or two species) with at least 105 bacteria/ml, with or without clinical symptoms led to the diagnosis of urinary tract infection.A vascular catheter infection has been suggested in the presence of inflammation, lymphangitis or purulent discharge at the catheter insertion site.The diagnosis of sepsis was evoked in the presence of fever or chills and at least one positive blood culture.

Statistical analysis
The SPSS IBM Version 16 software was used for statistical data analysis.Categorically measured variables were described using frequencies and percentages, and quantitative variables using means and standard deviation.The chi-squared test of independence was used to assess associations between categorically measured variables.The level of two-tailed significance was set at p ≤ 0.05.

Ethical consideration
The anonymity and confidentiality were respected.The identification of patients was done using a hospitalization number in order to collect the results of the bacteriological examinations.

Antimicrobial prescription
Among our patients, 446 (50.3%) were receiving at least one antimicrobial drug.These latter were prescribed for a community-acquired infection in 22.5% of patients, for a prophylactic indication in 21.1% and for a HAI in 8.6% (Table 1).

Prevalence of HAIs
86 patients had at least one HAI, corresponding to a prevalence of 9.7% with a 95% confidence interval of (7.7%; 11.6%).

HAIs' associated factors
The presence of HAI was significantly associated with the presence of invasive medical device (p<0.001), the presence of two medical devices or more (p<0.001),a higher ASA score (p<0.001) and a longer hospital stay (p<0.001)(Table 3).

SSI-associated factors
The presence of SSI was significantly associated with the class of contamination (p = 0.006) and not taking antibiotic prophylaxis (p = 0.014) (

Discussion
The current study is the fifth HAI PPS carried out in the IRUHC, Casablanca, Morocco.The prevalence of HAI was 10.3% in the PPS of 2014, 5.4% in the PPS of 2017 and 9.7% in the present study conducted in post-COVID-19 pandemic period [11,12].
The COVID-19 pandemic has placed substantial burdens on healthcare systems and hospitals worldwide.Healthcare workers' burnout, higher than usual hospitalizations and shortages in equipment might have impacted infection prevention efforts and common HAI rates.A previous study of US hospitals has shown that certain HAIs increased during the pandemic [13].Similar results were reported by a study conducted in seven resource-limited countries and a Dutch study [14,15].Conversely, other studies has shown that the pandemic has led to enhanced infection prevention efforts and a reduction in HAI rates during the ongoing pandemic [16][17][18].
The highest prevalence of HAIs in our study was observed in ICUs, which is consistent with the local PPS of 2017 and other studies [12,[19][20][21].Hemato-oncology departments came in second position in our study with a HAI prevalence of 18.3%.This may be due to the high use of invasive devices and the high frequency of immunocompromised patients in these departments.In fact, neutropenia, chemotherapy and central venous catheterization have been identified as risk factors implicated in the occurrence of HAI [22,23].
Similarly to results reported in the local PPS of 2017, nosocomial pneumonia, SSI and BSI were the most common sites of HAI in this study [12].However, in the local PPS of 2014 urinary tract infection was the main HAI [11].SSI and BSI were the most common HAIs reported in African studies according to a systematic review [24].
High rates of SSI were reported by different studies [20,[25][26][27].Appropriate perioperative antibiotic prophylaxis is an important component of SSI prevention.Centers for Disease Control and Prevention Guideline for the Prevention of Surgical Site Infection (2017) included three measures related to perioperative antibiotic prophylaxis: timing, drug appropriateness and drug discontinuation after surgery [28].
The main microorganism isolated in our patients with HAI was Acinetobacter baumannii, and all isolated strains were imipenem-resistant.Acinetobacter baumannii is an opportunistic human pathogen that predominantly infects critically ill patients.It is considered a global threat for the healthcare system, mainly due to its tendency to acquire multidrug resistance phenotypes at high rates [29,30].Infections caused by Acinetobacter baumannii account for nearly 2% of all HAIs in the United States and Europe [31,32].However, this proportion is twice as high in Asia and the Middle East [32].Although infection rates are lower than those caused by other Gram-negative pathogens, globally, nearly 45% of all isolates are considered to be MDR, with a proportion as high as 70% in Latin America and the Middle East [29].These MDR proportions are nearly four times higher than those observed for other Gram-negative pathogens, such as Pseudomonas aeruginosa and Klebsiella pneumoniae [29].Recently, carbapenem-resistant Acinetobacter baumannii has been added to the WHO published list of bacteria for which new antibiotics are urgently needed to address growing global resistance [33].
The prevalence of antimicrobial use slightly increased from 2017 to 2021, from 46.5% to 50.3%, respectively.
A multicenter Ethiopian study conducted in 2021 reported a higher prevalence of Antibiotic use of 63.8% [34].These results has practical and policy implications for strengthening antimicrobial stewardship programs and promoting rational antibiotics use.
In our study, the main antibiotics prescribed were penicillin A-beta-lactamase inhibitors association, thirdgeneration cephalosporins, aminoglycosides and fluoroquinolones.Similar results were reported by a global PPS conducted in 2015, including 53 countries from low, high and middle-income countries, with the highest prevalence of antibiotic prescription being in Africa [35].
In our study, Identified risk factors for HAIs were longer hospital stay, the presence of an invasive medical device, and high ASA score.Similar results were reported in the two previous local PPS [11,12].Regarding factors significantly associated with SSI, we have identified the class of contamination (p=0.006) and not taking antibiotic prophylaxis (p=0.014).Similar results were reported by other studies [36][37][38].Other risk factors have been reported in the literature such as the duration of surgery, length of preoperative hospital stay and ASA score [36][37][38].
Robust surveillance system is essential to the implementation of effective interventions and to assess the effectiveness of IPC programs.As described by the WHO, the core components of an effective IPC program include: establishing guidelines; supporting education and training; establishing HAI surveillance; using multimodal strategies; monitoring and evaluation of IPC practices; adequate staffing according to workload; adequate availability of materials and equipment for IPC [39].
This study has some limitations.It is a cross-sectional study, which is likely to underestimate the burden of HAIs.However, point prevalence surveys are cost-effective and allow the collection of a greater amount of information in a shorter period of time than incidence studies.Underestimation of HAI prevalence could also be a result of information bias, which may be due to interobserver variation in case definition or failure to identify HAIs due to limited or absent microbiology results for some patients.Another limitation is that the sample is not statistically representative of the general population, as our sample was drawn from a specific population hospitalized in a tertiary hospital, which may be vulnerable.However, the sample size was quite large, with 887 patients included in the analysis.

Conclusions
The emergence of imipenem-resistant Acinetobacter baumannii (IRAB) represents a serious therapeutic and epidemiological problem requiring the establishment of a system for monitoring the microbial environment and the application of strict hygiene measures.
Following the results of this study, the hospital hygiene department of the IRUHC set up an improvement program including a set of operational objectives.The first objective is to provide training and awareness in hospital hygiene for medical and paramedical staff and students.Continuous monitoring of the incidence of HAIs and cases of MDR bacteria infections must be ensured in all hospital departments.In addition, daily monitoring of waste management, bio-cleaning, and laundry management must be ensured to control the risk related to the environment.
this article Lyazidi S, Ouhadous M, Arai M, et al. (August 19, 2024) Prevalence of Healthcare-Associated Infections in a Tertiary Hospital in Casablanca, Morocco, 2021.Cureus 16(8): e67171.DOI 10.7759/cureus.67171dedicated to providing care to critical cases of COVID-19 requiring the resuscitation or intensive care.Alongside their usual activities, health professionals working in the IRUHC participated in the care of COVID-19 patients.The nosocomial infection control committee of IRUHC and the hospital hygiene service organized the fifth HAI point prevalence study (PPS) in the post-COVID-19 pandemic period.The objective of this study was to estimate the prevalence and identify associated factors of HAIs in IRUHC of Casablanca during the pandemic.